Brent R. Helliker

C4 photosynthesis, atmospheric CO2, and climate

Abstract The objectives of this synthesis are (1) to review the factors that influence the ecological, geographical, and palaeoecological distributions of plants possessing C4 photosynthesis and (2) to propose a hypothesis/model to explain both the distribution of C4 plants with respect to temperature and CO2 and why C4 photosynthesis is relatively uncommon in dicotyledonous plants (hereafter dicots), especially in comparison with its widespread distribution in monocotyledonous species (hereafter monocots). Our goal is to stimulate discussion of the factors controlling distributions of C4 plants today, historically, and under future elevated CO2 environments. Understanding the distributions of C3/C4 plants impacts not only primary productivity, but also the distribution, evolution, and migration of both invertebrates and vertebrates that graze on these plants. Sixteen separate studies all indicate that the current distributions of C4 monocots are tightly correlated with temperature: elevated temperatures during the growing season favor C4 monocots. In contrast, the seven studies on C4 dicot distributions suggest that a different environmental parameter, such as aridity (combination of temperature and evaporative potential), more closely describes their distributions. Differences in the temperature dependence of the quantum yield for CO2 uptake (light-use efficiency) of C3 and C4 species relate well to observed plant distributions and light-use efficiency is the only mechanism that has been proposed to explain distributional differences in C3/C4 monocots. Modeling of C3 and C4 light-use efficiencies under different combinations of atmospheric CO2 and temperature predicts that C4-dominated ecosystems should not have expanded until atmospheric CO2 concentrations reached the lower levels that are thought to have existed beginning near the end of the Miocene. At that time, palaeocarbonate and fossil data indicate a simultaneous, global expansion of C4-dominated grasslands. The C4 monocots generally have a higher quantum yield than C4 dicots and it is proposed that leaf venation patterns play a role in increasing the light-use efficiency of most C4 monocots. The reduced quantum yield of most C4 dicots is consistent with their rarity, and it is suggested that C4 dicots may not have been selected until CO2 concentrations reached their lowest levels during glacial maxima in the Quaternary. Given the intrinsic light-use efficiency advantage of C4 monocots, C4 dicots may have been limited in their distributions to the warmest ecosystems, saline ecosystems, and/or to highly disturbed ecosystems. All C4 plants have a significant advantage over C3 plants under low atmospheric CO2 conditions and are predicted to have expanded significantly on a global scale during full-glacial periods, especially in tropical regions. Bog and lake sediment cores as well as pedogenic carbonates support the hypothesis that C4 ecosystems were more extensive during the last glacial maximum and then decreased in abundance following deglaciation as atmospheric CO2 levels increased.

Subtropical to boreal convergence of tree-leaf temperatures.

The oxygen isotope ratio (δ18O) of cellulose is thought to provide a record of ambient temperature and relative humidity during periods of carbon assimilation. Here we introduce a method to resolve tree-canopy leaf temperature with the use of δ18O of cellulose in 39 tree species. We show a remarkably constant leaf temperature of 21.4 ± 2.2 °C across 50° of latitude, from subtropical to boreal biomes. This means that when carbon assimilation is maximal, the physiological and morphological properties of tree branches serve to raise leaf temperature above air temperature to a much greater extent in more northern latitudes. A main assumption underlying the use of δ18O to reconstruct climate history is that the temperature and relative humidity of an actively photosynthesizing leaf are the same as those of the surrounding air. Our data are contrary to that assumption and show that plant physiological ecology must be considered when reconstructing climate through isotope analysis. Furthermore, our results may explain why climate has only a modest effect on leaf economic traits in general.

Methane flux in non‐wetland soils in response to nitrogen addition: a meta‐analysis

The controls on methane (CH4) flux into and out of soils are not well understood. Environmental variables including temperature, precipitation, and nitrogen (N) status can have strong effects on the magnitude and direction (e.g., uptake vs. release) of CH4 flux. To better understand the interactions between CH4-cycling microorganisms and N in the non-wetland soil system, a meta-analysis was performed on published literature comparing CH4 flux in N amended and matched control plots. An appropriate study index was developed for this purpose. It was found that smaller amounts of N tended to stimulate CH4 uptake while larger amounts tended to inhibit uptake by the soil. When all other variables were accounted for, the switch occurred at 100 kg N x ha(-1) x yr(-1). Managed land and land with a longer duration of fertilization showed greater inhibition of CH4 uptake with added N. These results support the hypotheses that large amounts of available N can inhibit methanotrophy, but also that methanotrophs in upland soils can be N limited in their consumption of CH4 from the atmosphere. There were interactions between other variables and N addition on the CH4 flux response: lower temperature and, to a lesser extent, higher precipitation magnified the inhibition of CH4 uptake due to N addition. Several mechanisms that may cause these trends are discussed, but none could be conclusively supported with this approach. Further controlled and in situ study should be undertaken to isolate the correct mechanism(s) responsible and to model upland CH4 flux.

Differential 18O enrichment of leaf cellulose in C3 versus C4 grasses

We show that differences in the oxygen isotope ratio of leaf water between C3 and C4 grasses (five species of each photosynthetic type) become less distinct as relative humidity increases, and that 18O leaf water differences translate directly to the oxygen isotope ratio of leaf cellulose. A conceptual model is presented that is based on grass blade growth characteristics and observed patterns of progressive enrichment in grasses. The Barbour and Farquhar (2000) model was capable of explaining the oxygen isotope ratio of bulk leaf cellulose of C3 and C4 grasses grown under a variety of growth conditions.

The contribution of C3 and C4 plants to the carbon cycle of a tallgrass prairie: an isotopic approach.

The photosynthetic pathway composition (C3:C4 mixture) of an ecosystem is an important controller of carbon exchanges and surface energy flux partitioning, and therefore represents a fundamental ecophysiological distinction. To assess photosynthetic mixtures at a tallgrass prairie pasture in Oklahoma, we collected nighttime above-canopy air samples along concentration and isotopic gradients throughout the 1999 and 2000 growing seasons. We analyzed these samples for their CO2 concentration and carbon isotopic composition and calculated C3:C4 proportions with a two-source mixing model. In 1999, the C4 percentage increased from 38% in spring (late April) to 86% in early fall (mid-September). The C4 percentages inferred from ecosystem respiration measurements in 2000 indicate a smaller shift, from 67% in spring (early May) to 77% in mid-summer (late July). We also sampled daytime CO2 concentration and carbon isotope gradients above the canopy to determine ecosystem discrimination against 13CO2 during net uptake. These discrimination values were always lower than corresponding nighttime ecosystem respiration isotopic signatures would suggest. After accounting for the isotopic disequilibria between respiration and photosynthesis resulting from seasonal variations in the C3:C4 mixture, we estimated canopy photosynthetic discrimination. The C4 percentage calculated from this approach agrees with the percentage determined from nighttime respiration for sampling periods in both growing seasons. Isotopic imbalances between photosynthesis and respiration are likely to be common in mixed C3:C4 ecosystems and must be considered when using daytime isotopic measurements to constrain ecosystem physiology. Given the global extent of such ecosystems, isotopic imbalances likely contribute to global variations in the carbon isotopic composition of atmospheric CO2.

Estimates of net CO2 flux by application of equilibrium boundary layer concepts to CO2 and water vapor measurements from a tall tower

fluxes that affects the CO2 and water vapor mixing ratios. We apply quasi-equilibrium concepts for the terrestrial ABL to measurements of CO2 and water vapor made within the ABL from a tall tower (396 m) in Wisconsin. We suppose that CO2 and water vapor mixing ratios in the ABL approach an equilibrium on timescales longer than a day: a balance between the surface fluxes and the exchange with the free troposphere above. By using monthly averaged ABL-to-free-tropospheric water vapor differences and surface water vapor flux, realistic estimates of vertical velocity exchange with the free troposphere can be obtained. We then estimated the net surface flux of CO2 on a monthly basis for the year of 2000, using ABL-to-free-tropospheric CO2 differences, and our flux difference estimate of the vertical exchange. These ABL-scale estimates of net CO2 flux gave close agreement with eddy covariance measurements. Considering the large surface area which affects scalars in the ABL over synoptic timescales, the flux difference approach presented here could potentially provide regional-scale estimates of net CO2 flux. INDEX TERMS: 1615 Global Change: Biogeochemical processes (4805); 1818 Hydrology: Evapotranspiration; 3307 Meteorology and Atmospheric Dynamics: Boundary layer processes; 3322 Meteorology and Atmospheric Dynamics: Land/atmosphere interactions; KEYWORDS: boundary layer, CO2 exchange, evapotranspiration

Transpiration rate relates to within- and across-species variations in effective path length in a leaf water model of oxygen isotope enrichment

Stable oxygen isotope ratio of leaf water (δ(18)O(L)) yields valuable information on many aspects of plant-environment interactions. However, current understanding of the mechanistic controls on δ(18)O(L) does not provide complete characterization of effective path length (L) of the Péclet effect,--a key component of the leaf water model. In this study, we collected diurnal and seasonal series of leaf water enrichment and estimated L in six field-grown angiosperm and gymnosperm tree species. Our results suggest a pivotal role of leaf transpiration rate (E) in driving both within- and across-species variations in L. Our observation of the common presence of an inverse scaling of L with E in the different species therefore cautions against (1) the conventional treatment of L as a species-specific constant in leaf water or cellulose isotope (δ(18)O(p)) modelling; and (2) the use of δ(18)O(p) as a proxy for gs or E under low E conditions. Further, we show that incorporation of a multi-species L-E scaling into the leaf water model has the potential to both improve the prediction accuracy and simplify parameterization of the model when compared with the conventional approach. This has important implications for future modelling of oxygen isotope ratios.

Plant response to climate change varies with topography, interactions with neighbors, and ecotype

Predicting the future of any given species represents an unprecedented challenge in light of the many environmental and biological factors that affect organismal performance and that also interact with drivers of global change. In a three-year experiment set in the Mongolian steppe, we examined the response of the common grass Festuca lenensis to manipulated temperature and water while controlling for topographic variation, plant-plant interactions, and ecotypic differentiation. Plant survival and growth responses to a warmer, drier climate varied within the landscape. Response to simulated increased precipitation occurred only in the absence of neighbors, demonstrating that plant-plant interactions can supersede the effects of climate change. F. lenensis also showed evidence of local adaptation in populations that were only 300 m apart. Individuals from the steep and dry upper slope showed a higher stress/drought tolerance, whereas those from the more productive lower slope showed a higher biomass production and a greater ability to cope with competition. Moreover, the response of this species to increased precipitation was ecotype specific, with water addition benefiting only the least stress-tolerant ecotype from the lower slope origin. This multifaceted approach illustrates the importance of placing climate change experiments within a realistic ecological and evolutionary framework. Existing sources of variation impacting plant performance may buffer or obscure climate change effects.

Stable isotopes in leaf water of terrestrial plants

Leaf water contains naturally occurring stable isotopes of oxygen and hydrogen in abundances that vary spatially and temporally. When sufficiently understood, these can be harnessed for a wide range of applications. Here, we review the current state of knowledge of stable isotope enrichment of leaf water, and its relevance for isotopic signals incorporated into plant organic matter and atmospheric gases. Models describing evaporative enrichment of leaf water have become increasingly complex over time, reflecting enhanced spatial and temporal resolution. We recommend that practitioners choose a model with a level of complexity suited to their application, and provide guidance. At the same time, there exists some lingering uncertainty about the biophysical processes relevant to patterns of isotopic enrichment in leaf water. An important goal for future research is to link observed variations in isotopic composition to specific anatomical and physiological features of leaves that reflect differences in hydraulic design. New measurement techniques are developing rapidly, enabling determinations of both transpired and leaf water δ(18) O and δ(2) H to be made more easily and at higher temporal resolution than previously possible. We expect these technological advances to spur new developments in our understanding of patterns of stable isotope fractionation in leaf water.

Regulation of Rubisco activity in crassulacean acid metabolism plants: better late than never

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. The diurnal regulation of Rubisco was compared for a range of crassulacean acid metabolism (CAM) species in the context of high carboxylation and electron transport capacities, which may be an order of magnitude greater than rates of net CO2 uptake. Early in the light period, Rubisco activity and electron transport were limited when phosphoenolpyruvate carboxylase (PEPC) may have been operating, and maximal extractable activities and activation state for Rubisco were achieved at the end of Phase III, prior to the direct atmospheric uptake of CO2 during Phase IV. The delayed activation was associated with levels of Rubisco activase protein, which reached a maximum at midday, and may account for this pattern of Rubisco activation. This regulation may be modified by environmental conditions - processes that tend to restrict PEPC activity, such as drought stress or incubation of leaves overnight in an oxygen-free atmosphere, release Rubisco from inhibition early in the light period. The quantum yield of light use also tracks Rubisco carboxylation, being particularly low at dawn when PEPC is active. The plasticity in expression of the CAM cycle is therefore matched by the regulation of key carboxylases, with extractable Rubisco activity maximal when drawdown of atmospheric CO2 to cells in succulent CAM tissues is most likely to limit photon utilization shortly after midday, during Phase IV.